Molecular dissection of CHARGE syndrome highlights the vulnerability of neural crest cells to problems with alternative splicing and other transcription-related processes

References

• Lehalle D, Wieczorek D, Zechi-Ceide RM, et al. A review of craniofacial disorders caused by spliceosomal defects. Clin Genet. 2015 Nov;88(5):405–415. PubMed PMID: 25865758.
   PubMed Web of Science ®Google Scholar
• Scotti MM, Swanson MS. RNA mis-splicing in disease. Nat Rev Genet. 2016 Jan;17(1):19–32. . PubMed PMID: 26593421.
   PubMed Web of Science ®Google Scholar
• Czeschik JC, Voigt C, Alanay Y, et al. Clinical and mutation data in 12 patients with the clinical diagnosis of Nager syndrome. Hum Genet. 2013 Aug;132(8):885–898. PubMed PMID: 23568615.
   PubMed Web of Science ®Google Scholar
• Rudnik-Schoneborn S, Heller R, Berg C, et al. Congenital heart disease is a feature of severe infantile spinal muscular atrophy. J Med Genet. 2008 Oct;45(10):635–638. PubMed PMID: 18662980.
   PubMed Web of Science ®Google Scholar
• Tsuiji H, Iguchi Y, Furuya A, et al. Spliceosome integrity is defective in the motor neuron diseases ALS and SMA. EMBO Mol Med. 2013 Feb;5(2):221–234. PubMed PMID: 23255347; PubMed Central PMCID: PMCPMC3569639.
   PubMed Web of Science ®Google Scholar
• Wieczorek D. Human facial dysostoses. Clin Genet. 2013 Jun;83(6):499–510. . PubMed PMID: 23565775.
   PubMed Web of Science ®Google Scholar
• Bronner ME, LeDouarin NM. Development and evolution of the neural crest: an overview. Dev Biol. 2012 Jun 1;366(1):2–9. . PubMed PMID: 22230617; PubMed Central PMCID: PMC3351559.
   PubMed Web of Science ®Google Scholar
• Bolande RP. Neurocristopathy: its growth and development in 20 years. Pediatr Pathol Lab Med. 1997 Jan-Feb;17(1):1–25. PubMed PMID: 9050057.
   PubMed Web of Science ®Google Scholar
• Etchevers HC, Amiel J, Lyonnet S. Molecular bases of human neurocristopathies. Adv Exp Med Biol. 2006;589:213–234. . PubMed PMID: 17076285.
   PubMed Web of Science ®Google Scholar
• Hsu P, Ma A, Wilson M, et al. CHARGE syndrome: a review. J Paediatr Child Health. 2014 Jul;50(7):504–511. PubMed PMID: 24548020.
   PubMed Web of Science ®Google Scholar
• Hale CL, Niederriter AN, Green GE, et al. Atypical phenotypes associated with pathogenic CHD7 variants and a proposal for broadening CHARGE syndrome clinical diagnostic criteria. Am J Med Genet A. 2016 Feb;170(2):344–354. PubMed PMID: 26590800.
   Web of Science ®Google Scholar
• Vissers LE, van Ravenswaaij CM, Admiraal R, et al. Mutations in a new member of the chromodomain gene family cause CHARGE syndrome. Nat Genet. 2004 Sep;36(9):955–957. PubMed PMID: 15300250.
   PubMed Web of Science ®Google Scholar
• Bouazoune K, Kingston RE. Chromatin remodeling by the CHD7 protein is impaired by mutations that cause human developmental disorders. Proc Natl Acad Sci U S A. 2012 Nov 20;109(47):19238–19243. . PubMed PMID: 23134727; PubMed Central PMCID: PMC3511097.
   PubMed Web of Science ®Google Scholar
• Schnetz MP, Handoko L, Akhtar-Zaidi B, et al. CHD7 targets active gene enhancer elements to modulate ES cell-specific gene expression. PLoS Genet. 2010 Jul;6(7):e1001023. PubMed PMID: 20657823; PubMed Central PMCID: PMC2904778.
   PubMed Web of Science ®Google Scholar
• Bajpai R, Chen DA, Rada-Iglesias A, et al. CHD7 cooperates with PBAF to control multipotent neural crest formation. Nature. 2010 Feb 18;463(7283):958–962. PubMed PMID: 20130577; PubMed Central PMCID: PMC2890258.
   PubMed Web of Science ®Google Scholar
• Fujita K, Ogawa R, Ito K. CHD7, Oct3/4, Sox2, and Nanog control FoxD3 expression during mouse neural crest-derived stem cell formation. The FEBS Journal. 2016 Oct;283(20):3791–3806. . PubMed PMID: 27579714.
   PubMed Web of Science ®Google Scholar
• Schulz Y, Wehner P, Opitz L, et al. CHD7, the gene mutated in CHARGE syndrome, regulates genes involved in neural crest cell guidance. Hum Genet. 2014 Aug;133(8):997–1009. PubMed PMID: 24728844.
   PubMed Web of Science ®Google Scholar
• Bergeron KF, Cardinal T, Toure AM, et al. Male-biased aganglionic megacolon in the tasht mouse line due to perturbation of silencer elements in a large gene desert of chromosome 10. PLoS Genet. 2015 Mar;11(3):e1005093. PubMed PMID: 25786024.
   PubMed Web of Science ®Google Scholar
• Bergeron KF, Nguyen CM, Cardinal T, et al. Upregulation of the Nr2f1-A830082K12Rik gene pair in murine neural crest cells results in a complex phenotype reminiscent of waardenburg syndrome type 4. Disease Models & Mechanisms. 2016 Nov 2;9(11):1283–1293. PubMed PMID: 27585883.
   PubMed Web of Science ®Google Scholar
• Pilon N. Pigmentation-based insertional mutagenesis is a simple and potent screening approach for identifying neurocristopathy-associated genes in mice. Rare Dis. 2016;4(1):e1156287.
   PubMed Web of Science ®Google Scholar
• Soret R, Mennetrey M, Bergeron KF, et al. A collagen VI-dependent pathogenic mechanism for Hirschsprung’s disease. J Clin Invest. 2015 Dec 1;125(12):4483–4496. PubMed PMID: 26571399.
   PubMed Web of Science ®Google Scholar
• Belanger C, Berube-Simard FA, Leduc E, et al. Dysregulation of cotranscriptional alternative splicing underlies CHARGE syndrome. Proc Natl Acad Sci U S A. 2018 Jan 23;115(4):E620–E629. PubMed PMID: 29311329; PubMed Central PMCID: PMC5789929.
   PubMed Web of Science ®Google Scholar
• Buker SM, Iida T, Buhler M, et al. Two different Argonaute complexes are required for siRNA generation and heterochromatin assembly in fission yeast. Nat Struct Mol Biol. 2007 Mar;14(3):200–207. PubMed PMID: 17310250.
   PubMed Web of Science ®Google Scholar
• Ameyar-Zazoua M, Rachez C, Souidi M, et al. Argonaute proteins couple chromatin silencing to alternative splicing. Nat Struct Mol Biol. 2012 Oct;19(10):998–1004. PubMed PMID: 22961379.
   PubMed Web of Science ®Google Scholar
• Munding EM, Shiue L, Katzman S, et al. Competition between pre-mRNAs for the splicing machinery drives global regulation of splicing. Mol Cell. 2013 Aug 08;51(3):338–348. PubMed PMID: 23891561; PubMed Central PMCID: PMC3771316.
   PubMed Web of Science ®Google Scholar
• Luco RF, Allo M, Schor IE, et al. Epigenetics in alternative pre-mRNA splicing. Cell. 2011 Jan 7;144(1):16–26. PubMed PMID: 21215366; PubMed Central PMCID: PMC3038581.
   PubMed Web of Science ®Google Scholar
• Naftelberg S, Schor IE, Ast G, et al. Regulation of alternative splicing through coupling with transcription and chromatin structure. Annu Rev Biochem. 2015;84:165–198. . PubMed PMID: 26034889.
   PubMed Web of Science ®Google Scholar
• Allo M, Buggiano V, Fededa JP, et al. Control of alternative splicing through siRNA-mediated transcriptional gene silencing. Nat Struct Mol Biol. 2009 Jul;16(7):717–724. PubMed PMID: 19543290.
   PubMed Web of Science ®Google Scholar
• Kalantari R, Chiang CM, Corey DR. Regulation of mammalian transcription and splicing by Nuclear RNAi. Nucleic Acids Res. 2016 Jan 29;44(2):524–537. . PubMed PMID: 26612865; PubMed Central PMCID: PMC4737150.
   PubMed Web of Science ®Google Scholar
• Saint-Andre V, Batsche E, Rachez C, et al. Histone H3 lysine 9 trimethylation and HP1gamma favor inclusion of alternative exons. Nat Struct Mol Biol. 2011 Mar;18(3):337–344. PubMed PMID: 21358630.
   PubMed Web of Science ®Google Scholar
• Gompers AL, Su-Feher L, Ellegood J, et al. Germline Chd8 haploinsufficiency alters brain development in mouse. Nat Neurosci. 2017 Aug;20(8):1062–1073. PubMed PMID: 28671691; PubMed Central PMCID: PMCPMC6008102.
   PubMed Web of Science ®Google Scholar
• Murawska M, Brehm A. CHD chromatin remodelers and the transcription cycle. Transcription. 2011 Nov-Dec;2(6):244–253. . PubMed PMID: 22223048; PubMed Central PMCID: PMCPMC3265784.
   PubMedGoogle Scholar
• Sims RJ 3rd, Millhouse S, Chen CF, et al. Recognition of trimethylated histone H3 lysine 4 facilitates the recruitment of transcription postinitiation factors and pre-mRNA splicing. Mol Cell. 2007 Nov 30;28(4):665–676. PubMed PMID: 18042460; PubMed Central PMCID: PMC2276655.
   PubMed Web of Science ®Google Scholar
• Tai HH, Geisterfer M, Bell JC, et al. CHD1 associates with NCoR and histone deacetylase as well as with RNA splicing proteins. Biochem Biophys Res Commun. 2003 Aug 15;308(1):170–176. PubMed PMID: 12890497.
   PubMed Web of Science ®Google Scholar
• Allemand E, Myers MP, Garcia-Bernardo J, et al. A Broad Set of Chromatin Factors Influences Splicing. PLoS Genet. 2016 Sep;12(9):e1006318. PubMed PMID: 27662573; PubMed Central PMCID: PMC5035054.
   PubMed Web of Science ®Google Scholar
• Jordan VK, Fregeau B, Ge X, et al. Genotype-phenotype correlations in individuals with pathogenic RERE variants. Hum Mutat. 2018 May;39(5):666–675. PubMed PMID: 29330883; PubMed Central PMCID: PMCPMC5903952.
   PubMed Web of Science ®Google Scholar
• Moccia A, Srivastava A, Skidmore JM, et al. Genetic analysis of CHARGE syndrome identifies overlapping molecular biology. Genet Med. 2018 Jan 4. DOI:10.1038/gim.2017.233. PubMed PMID: 29300383; PubMed Central PMCID: PMCPMC6034995.
   PubMed Web of Science ®Google Scholar
• Hastings ML, Allemand E, Duelli DM, et al. Control of pre-mRNA splicing by the general splicing factors PUF60 and U2AF(65). PLoS One. 2007 Jun 20;2(6):e538. PubMed PMID: 17579712; PubMed Central PMCID: PMCPMC1888729.
   PubMed Web of Science ®Google Scholar
• Page-McCaw PS, Amonlirdviman K, Sharp PA. PUF60: a novel U2AF65-related splicing activity. Rna. 1999 Dec;5(12):1548–1560. PubMed PMID: 10606266; PubMed Central PMCID: PMCPMC1369877.
   PubMed Web of Science ®Google Scholar
• Duskova E, Hnilicova J, Stanek D. CRE promoter sites modulate alternative splicing via p300-mediated histone acetylation. RNA Biology. 2014;11(7):865–874. . PubMed PMID: 25019513; PubMed Central PMCID: PMCPMC4179961.
   PubMed Web of Science ®Google Scholar
• Plaster N, Sonntag C, Schilling TF, et al. REREa/Atrophin-2 interacts with histone deacetylase and Fgf8 signaling to regulate multiple processes of zebrafish development. Dev Dyn. 2007 Jul;236(7):1891–1904. PubMed PMID: 17576618.
   PubMed Web of Science ®Google Scholar
• Zhang S, Xu L, Lee J, et al. Drosophila atrophin homolog functions as a transcriptional corepressor in multiple developmental processes. Cell. 2002 Jan 11;108(1):45–56. PubMed PMID: 11792320.
   PubMed Web of Science ®Google Scholar
• Zoltewicz JS, Stewart NJ, Leung R, et al. Atrophin 2 recruits histone deacetylase and is required for the function of multiple signaling centers during mouse embryogenesis. Development. 2004 Jan;131(1):3–14. PubMed PMID: 14645126.
   PubMed Web of Science ®Google Scholar
• Jongmans MC, van Ravenswaaij-Arts CM, Pitteloud N, et al. CHD7 mutations in patients initially diagnosed with Kallmann syndrome–the clinical overlap with CHARGE syndrome. Clin Genet. 2009 Jan;75(1):65–71. PubMed PMID: 19021638; PubMed Central PMCID: PMC2854009.
   PubMed Web of Science ®Google Scholar
• Ogata T, Fujiwara I, Ogawa E, et al. Kallmann syndrome phenotype in a female patient with CHARGE syndrome and CHD7 mutation. Endocr J. 2006 Dec;53(6):741–743. PubMed PMID: 16960397.
   PubMed Web of Science ®Google Scholar
• Gordon CT, Petit F, Oufadem M, et al. EFTUD2 haploinsufficiency leads to syndromic oesophageal atresia. J Med Genet. 2012 Dec;49(12):737–746. PubMed PMID: 23188108.
   PubMed Web of Science ®Google Scholar
• Bernier FP, Caluseriu O, Ng S, et al. Haploinsufficiency of SF3B4, a component of the pre-mRNA spliceosomal complex, causes Nager syndrome. Am J Hum Genet. 2012 May 04;90(5):925–933. PubMed PMID: 22541558; PubMed Central PMCID: PMC3376638.
   PubMed Web of Science ®Google Scholar
• Hutson MR, Keyte AL, Hernandez-Morales M, et al. Temperature-activated ion channels in neural crest cells confer maternal fever-associated birth defects. Sci Signal. 2017 Oct 10;10(500). PubMed PMID: 29018170. DOI:10.1126/scisignal.aal4055.
   PubMed Web of Science ®Google Scholar
• Smith SM, Garic A, Flentke GR, et al. Neural crest development in fetal alcohol syndrome. Birth Defects Research Part C, Embryo Today: Reviews. 2014 Sep;102(3):210–220. PubMed PMID: 25219761; PubMed Central PMCID: PMCPMC4827602.
   PubMedGoogle Scholar
• Bayless NL, Greenberg RS, Swigut T, et al. Zika virus infection induces cranial neural crest cells to produce cytokines at levels detrimental for neurogenesis. Cell Host Microbe. 2016 Oct 12;20(4):423–428. PubMed PMID: 27693308; PubMed Central PMCID: PMCPMC5113290.
   PubMed Web of Science ®Google Scholar
• Wang XY, Li S, Wang G, et al. High glucose environment inhibits cranial neural crest survival by activating excessive autophagy in the chick embryo. Scientific Reports. 2015 Dec;16(5):18321. . PubMed PMID: 26671447; PubMed Central PMCID: PMC4680872.
   PubMed Web of Science ®Google Scholar
• Morgan SC, Relaix F, Sandell LL, et al. Oxidative stress during diabetic pregnancy disrupts cardiac neural crest migration and causes outflow tract defects. Birth Defects Res A Clin Mol Teratol. 2008 Jun;82(6):453–463. PubMed PMID: 18435457; PubMed Central PMCID: PMCPMC5452612.
   PubMedGoogle Scholar
• Jones NC, Lynn ML, Gaudenz K, et al. Prevention of the neurocristopathy treacher collins syndrome through inhibition of p53 function. Nat Med. 2008 Feb;142:125–133. . PubMed PMID: 18246078; PubMed Central PMCID: PMC3093709. eng. nm1725 [pii].
   PubMed Web of Science ®Google Scholar
• Calo E, Gu B, Bowen ME, et al. Tissue-selective effects of nucleolar stress and rDNA damage in developmental disorders. Nature. 2018 Feb 1;554(7690):112–117. PubMed PMID: 29364875; PubMed Central PMCID: PMCPMC5927778.
   PubMed Web of Science ®Google Scholar
• Allende-Vega N, Dayal S, Agarwala U, et al. p53 is activated in response to disruption of the pre-mRNA splicing machinery. Oncogene. 2013 Jan 03;32(1):1–14. PubMed PMID: 22349816.
   PubMed Web of Science ®Google Scholar
• Van Nostrand JL, Brady CA, Jung H, et al. Inappropriate p53 activation during development induces features of CHARGE syndrome. Nature. 2014 Oct 9;514(7521):228–232. PubMed PMID: 25119037; PubMed Central PMCID: PMC4192026.
   PubMed Web of Science ®Google Scholar
• Balow SA, Pierce LX, Zentner GE, et al. Knockdown of fbxl10/kdm2bb rescues chd7 morphant phenotype in a zebrafish model of CHARGE syndrome. Dev Biol. 2013 Oct 01;382(1):57–69. PubMed PMID: 23920116; PubMed Central PMCID: PMC3816111.
   PubMed Web of Science ®Google Scholar
• Fiszbein A, Kornblihtt AR. Alternative splicing switches: important players in cell differentiation. Bioessays. 2017 Jun;39(6). DOI:10.1002/bies.201600157. PubMed PMID: 28452057.
   PubMed Web of Science ®Google Scholar
• Weyn-Vanhentenryck SM, Feng H, Ustianenko D, et al. Precise temporal regulation of alternative splicing during neural development. Nat Commun. 2018 Jun 6;9(1):2189. 10.1038/s41467-018-04559-0. PubMed PMID: 29875359; PubMed Central PMCID: PMCPMC5989265.
   PubMedGoogle Scholar